Advertisement

DNA Mechanics and Topology

  • Sumitabha Brahmachari
  • John F. MarkoEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1092)

Abstract

We review the current understanding of the mechanics of DNA and DNA-protein complexes, from scales of base pairs up to whole chromosomes. Mechanics of the double helix as revealed by single-molecule experiments will be described, with an emphasis on the role of polymer statistical mechanics. We will then discuss how topological constraints— entanglement and supercoiling—impact physical and mechanical responses. Models for protein–DNA interactions, including effects on polymer properties of DNA of DNA-bending proteins will be described, relevant to behavior of protein–DNA complexes in vivo. We also discuss control of DNA entanglement topology by DNA-lengthwise-compaction machinery acting in concert with topoisomerases. Finally, the chapter will conclude with a discussion of relevance of several aspects of physical properties of DNA and chromatin to oncology.

Keywords

DNA mechanics DNA–protein interactions Supercoiling Plectoneme Braid Worm-like chain DNA topology Linking number Lengthwise compaction. 

References

  1. 1.
    Goodsell DS (1992) The machinery of life. Springer, New YorkGoogle Scholar
  2. 2.
    Feig M, Marko JF, Pettitt M (2003) Metal-ligand interactions. In: Russo N, Salahub DR, Witko M (eds) NATO science series II, vol 116. Kluwer Academic, Dordrecht, pp 193–204Google Scholar
  3. 3.
    Rybenkov VV, Cozzarelli NR, Vologodskii AV (1993) Proc Natl Acad Sci USA 11:5307CrossRefGoogle Scholar
  4. 4.
    Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM (1998) Science 282:902PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Maier B, Bensimon D, Croquette V (2000) Proc Natl Acad Sci USA 97:12002PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Hagerman PJ (1988) Annu Rev Biophys Biophys Chem 17:265PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Marko JF, Siggia ED (1995) Macromolecules 28:8759CrossRefGoogle Scholar
  8. 8.
    Yamakawa H, Stockmayer WH (1972) J Chem Phys 57:2843CrossRefGoogle Scholar
  9. 9.
    Schopflin R, Brutzer H, Muller O, Seidel R, Wedemann G (2012) Biophys J 103:323PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Du Q, Kotlyar A, Vologodskii A (2008) Nucleic Acids Res 36:1120PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Le TT, Kim HD (2014) Nucleic Acids Res 42:10786PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Nature 389:251PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Lowary PT, Widom J (1998) J Mol Biol 276:19PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JZ, Widom J (2006) Nature 442:772PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Marko JF (2005) Introduction to single-DNA micromechanics. In: Multiple aspects of DNA and RNA from biophysics to bioinformatics. Les Houches Session LXXXII. Elsevier, New York, pp 211–270Google Scholar
  16. 16.
    de Gennes P-G (1979) Scaling concepts in polymer physics. Sec. I.4.1. Cornell University Press, IthacaGoogle Scholar
  17. 17.
    Saleh OA, McIntosh DB, Pincus P, Ribeck N (2009) Phys Rev Lett 102:068301PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    McIntosh DB, Ribeck N, Saleh OA (2009) Phys Rev E 80:041803CrossRefGoogle Scholar
  19. 19.
    Neuman KC, Lionnet T, Allemand J-F (2007) Annu Rev Mater Res 37:33CrossRefGoogle Scholar
  20. 20.
    Yan J, Kawamura R, Marko JF (2005) Phys Rev E 71:061905CrossRefGoogle Scholar
  21. 21.
    Smith SB, Finzi L, Bustamante C (1992) Science 258:1122CrossRefPubMedGoogle Scholar
  22. 22.
    Odijk T (1995) Macromolecules 28:7016CrossRefGoogle Scholar
  23. 23.
    SantaLucia J Jr (1998) Proc Natl Acad Sci USA 95:1460PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Essevaz-Roulet B, Bockelmann U, Heslot F (1997) Proc Natl Acad USA 94:11935CrossRefGoogle Scholar
  25. 25.
    Bockelmann U, Thomen Ph, Viasnoff V, Heslot F (2002) Biophys J 82:1537PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Lubensky DK, Nelson DR (2000) Phys Rev Lett 85:1572PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Lubensky DK, Nelson DR (2002) Phys Rev E 65:031917CrossRefGoogle Scholar
  28. 28.
    Cluzel P, Lebrun A, Heller C, Lavery R, Viovy JL, Chatenay D, Caron F (1996) Science 271:792CrossRefPubMedGoogle Scholar
  29. 29.
    Smith SB, Cui Y, Bustamante C (1996) Science 271:795PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Strick TR, Bensimon D, Croquette V (1999) In: Bradbury EM, Pongor S (eds) Structural biology and functional genomics. NATO science series, vol 3. Kluwer Academic, Boston, pp 87–96Google Scholar
  31. 31.
    Bryant Z, Stone MD, Gore J, Cozzarelli NR, Bustamante C (2003) Nature 424:338PubMedCrossRefGoogle Scholar
  32. 32.
    Sheinin MY, Forth S, Marko JF, Wang MD (2011) Phys Rev Lett 107:108102PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Marko JF, Neukirch S (2013) Phys Rev E 88:062722CrossRefGoogle Scholar
  34. 34.
    Vologodskii AV, Marko JF (1997) Biophys J 73:123PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Landau LD, Lifshitz EM (1986) Theory of elasticity, Ch. II. Pergamon, New YorkGoogle Scholar
  36. 36.
    White JH (1969) Am J Math 91:693CrossRefGoogle Scholar
  37. 37.
    Fuller FB (1971) Proc Natl Acad Sci USA 68:815PubMedCrossRefGoogle Scholar
  38. 38.
    Marko JF, Siggia ED (1994) Science 265:506PubMedCrossRefGoogle Scholar
  39. 39.
    Marko JF, Siggia ED (1995) Phys Rev E 52:2912CrossRefGoogle Scholar
  40. 40.
    Marko JF, Neukirch S (2012) Phys Rev E 85:011908CrossRefGoogle Scholar
  41. 41.
    Helfrich W, Harbich W (1985) Chem Scr 25:32Google Scholar
  42. 42.
    Burkhardt TW (1997) J Phys A 30:L167CrossRefGoogle Scholar
  43. 43.
    Ubbink J, Odijk T (1999) Biophys J 76:2502PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Odijk T (1983) Macromolecules 16:1340CrossRefGoogle Scholar
  45. 45.
    Neukirch S, Marko JF (2011) Phys Rev Lett 106:138104PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Marko JF (2007) Phys Rev E 76:021926CrossRefGoogle Scholar
  47. 47.
    Moroz JD, Nelson P (1997) Proc Natl Acad Sci USA 94:14418PubMedCrossRefGoogle Scholar
  48. 48.
    Moroz JD, Nelson P (1998) Macromolecules 31:6333CrossRefGoogle Scholar
  49. 49.
    Strick TR, Allemand J-F, Bensimon D, Bensimon A, Croquette V (1996) Science 271:1835PubMedCrossRefGoogle Scholar
  50. 50.
    Fuller FB (1978) Proc Natl Acad Sci USA 75:3557PubMedCrossRefGoogle Scholar
  51. 51.
    Love AEH (1944) Treatise on the mathematical theory of elasticity, Sec. 264. Dover, New YorkGoogle Scholar
  52. 52.
    Banigan EJ, Marko JF (2014) Phys Rev E 89:062706CrossRefGoogle Scholar
  53. 53.
    Forth S, Sheinin MY, Daniels B, Sethna JP, Wang MD (2008) Phys Rev Lett 100:148301PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Mosconi F, Allemand JF, Bensimon D, Croquette V (2009) Phys Rev Lett 102:078301PubMedCrossRefGoogle Scholar
  55. 55.
    Zhang H, Marko JF (2008) Phys Rev E 77:031916CrossRefGoogle Scholar
  56. 56.
    Matek C, Ouldridge TE, Doye JPK, Louis AA (2015) Sci Rep 5:7655PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Ganji M, Kim SH, Van Der Torre J, Abbondanzieri E, Dekker C (2016) Nano Lett 16:4699PubMedCrossRefGoogle Scholar
  58. 58.
    Dittmore A, Brahmachari S, Takagi Y, Marko JF, Neuman KC (2017) Phys Rev Lett 119:147801PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Gowers DM, Halford SE (2003) EMBO J 22:1410PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Lomholt MA, van den Broek B, Kalisch SMJ, Wuite GJL, Metzler R (2009) Proc Natl Acad Sci USA 106:8204PubMedCrossRefGoogle Scholar
  61. 61.
    Hosfield DJ, Guan Y, Haas BJ, Cunningham RP, Tainer JA (1999) Cell 98:397PubMedCrossRefGoogle Scholar
  62. 62.
    Charvin G, Bensimon D, Croquette V (2003) Proc Natl Acad Sci USA 100:9820PubMedCrossRefGoogle Scholar
  63. 63.
    Stone MD, Bryant Z, Crisona NJ, Smith SB, Vologodskii A, Bustamante C, Cozzarelli NR (2003) Proc Natl Acad Sci USA 100:8654PubMedCrossRefGoogle Scholar
  64. 64.
    Neuman KC, Charvin G, Bensimon D, Croquette V (2009) Proc Natl Acad Sci USA 106:6986PubMedCrossRefGoogle Scholar
  65. 65.
    Bai H, Sun M, Ghosh P, Hatfull GF, Grindley NDF, Marko JF (2011) Proc Natl Acad Sci USA 108:7419PubMedCrossRefGoogle Scholar
  66. 66.
    Seol Y, Hardin AH, Strub MP, Charvin G, Neuman KC (2013)Nucleic Acids Res 41:4640PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Terekhova K, Marko JF, Mondragón A (2014) Nucleic Acids Res 42:11657PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Brahmachari S, Marko JF (2017) Phys Rev E 95:052401PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Charvin G, Vologodskii A, Bensimon D, Croquette V (2005) Biophys J 88:4124PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Argudo D, Purohit PK (2013) Math Mech Solids 18:649CrossRefGoogle Scholar
  71. 71.
    Brahmachari S, Gunn KH, Guintoli RD, Mondragón A, Marko JF (2017) Phys Rev Lett 119:188103PubMedCrossRefGoogle Scholar
  72. 72.
    Bancaud A, Conde e Silva N, Barbi M, Wagner G, Allemand JF, Mozziconacci J, Lavelle C, Croquette V, Victor JM, Prunell A, Viovy JL (2006) Nat Struct Mol Biol 13:444CrossRefGoogle Scholar
  73. 73.
    Bancaud A, Wagner G, Conde e Silva N, Lavelle C, Wong H, Mozziconacci J, Barbi M, Sivolob A, Le Cam E, Mouawad L, Viovy JL, Victor JM, Prunell A (2007) Mol Cell 27:135Google Scholar
  74. 74.
    Yan J, Magnasco MO, Marko JF (1999) Nature 401:932PubMedCrossRefGoogle Scholar
  75. 75.
    Vologodskii AV, Zhang W, Rybenkov VV, Podtelezhnikov AA, Subramanian D, Griffith JD, Cozzarelli NR (2001) Proc Natl Acad Sci USA 98:3045PubMedCrossRefGoogle Scholar
  76. 76.
    Koster DA, Crut A, Shuman S, Bjornsti MA, Dekker NH (2010) Cell 142:519PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Terekhova K, Marko JF, Mondragon A (2013) Biochem Soc Trans 41:571PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Rybenkov VV, Ullsperger C, Vologodskii AV, Cozzarelli NR (1997) Science 277:648CrossRefGoogle Scholar
  79. 79.
    Buck GR, Zechiedrich EL (2004) J Mol Biol 340:933PubMedCrossRefGoogle Scholar
  80. 80.
    Sumners DW, Whittington SG (1988) J Phys A Math Gen 21:1689CrossRefGoogle Scholar
  81. 81.
    Koniaris K, Muthukumar M (1991) Phys Rev Lett 66:2211PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Shaw SY, Wang JC (1993) Science 260:533PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    des Cloizeaux J (1981) J Phys (Paris) 42:L433Google Scholar
  84. 84.
    Tanaka F (1982) Prog Theor Phys 68:148–163; Prog Theor Phys 68:164–177CrossRefGoogle Scholar
  85. 85.
    Marko JF (2009) Phys Rev E 79:051905CrossRefGoogle Scholar
  86. 86.
    Baiesi M, Orlandini E, Stella AL (2001) Phys Rev Lett 87:070602PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Jun S, Mulder B (2006) Proc Natl Acad Sci USA 103:12388PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Pelletier J, Halvorsen K, Ha BY, Paparcone R, Sandler SJ, Woldringh CL, Wong WP, Jun S (2012) Proc Natl Acad Sci USA 109:2649CrossRefGoogle Scholar
  89. 89.
    Hadizadeh Yazdi N, Guet CC, Johnson RC, Marko JF (2012) Mol Microbiol 86:1318PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Marko JF (2011) J Stat Phys 142:1353PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Swinger KK, Lemburg KM, Zhang Y, Rice PA (2003) EMBO J 22:3749PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Grindley NDF, Whiteson KL, Rice PA (2006) Annu Rev Biochem 75:567PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Taneja B, Patel A, Slesarev A, Mondragon A (2006) EMBO J 25:398PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Halford SE, Marko JF (2004) Nucleic Acids Res 32:3040PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Parsaeian A, de la Cruz MO, Marko JF (2013) Phys Rev E 88:040703RCrossRefGoogle Scholar
  96. 96.
    Graham J, Marko JF (2011) Nucleic Acids Res 39:2249PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Loparo JJ, Kulczyk AW, Richardson CC, van Oijen AM (2011) Proc Natl Acad Sci USA 108:3584PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Joshi CP, Panda D, Martell DJ, Andoy NM, Chen TY, Gaballa A, Helmann JD, Chen P (2012) Proc Natl Acad Sci USA 109:15121PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
  100. 100.
    Gibb B, Ye LF, Gergoudis SC, Kwon Y, Niu H, Sung P, Greene EC (2014) PLOS One 9:e87922PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Giuntoli RD, Linzer NB, Banigan EJ, Sing CE, M. Olvera de la Cruz, Graham JS, Johnson RC, Marko JF (2015) J Mol Biol 427:3123Google Scholar
  102. 102.
    Kamar RI, Banigan EJ, Erbas A, Giuntoli RD, Olvera de la Cruz M, Johnson RC, Marko JF (2017) Proc Natl Acad Sci USA 114:E3251-7PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Hadizadeh N, Johnson RC, Marko JF (2016) J Bact 198:1735–1742PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Léger JF, Robert J, Bordieu L, Chatenay D, Marko JF (1998) Proc Natl Acad Sci USA 95:12295PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Marko JF, Siggia ED (1997) Biophys J 73:2173PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Sankararaman S, Marko JF (2005) Phys Rev E 71:021911CrossRefGoogle Scholar
  107. 107.
    Blumberg S, Tkachenko AV, Meiners JC (2005) Biophys J 88:1692PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Pope LH, Bennink ML, van Leijenhorst-Groener KA, Nikova D, Greve J, Marko JF (2005) Biophys J 88:3572PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Yan J, Maresca T, Skoko D, Adams CD, Xiao B, Christensen M, Heald R, Marko JF (2007) Mol Biol Cell 18:464PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Killian JL, Li M, Sheinin MY, Wang MD (2012) Curr Opin Struct Biol 22:80PubMedCrossRefGoogle Scholar
  111. 111.
    Rimsky S, Travers A (2011) Curr Opin Microbiol 14:136PubMedCrossRefGoogle Scholar
  112. 112.
    Ali BMJ, Amit R, Braslavsky I, Oppenheim AB, Gileadi O, Stavans J (2001) Proc Natl Acad Sci USA 98:10658PubMedCrossRefGoogle Scholar
  113. 113.
    van Noort J, Verbrugge S, Goosen N, Dekker C, Dame RT (2004) Proc Natl Acad Sci USA 101:6969PubMedCrossRefGoogle Scholar
  114. 114.
    Skoko D, Wong B, Johnson RC, Marko JF (2004) Biochemistry 43:13867PubMedCrossRefGoogle Scholar
  115. 115.
    Skoko D, Yoo D, Bai H, Schnurr B, Yan J, McLeod SM, Marko JF, Johnson RC (2006) J Mol Biol 36:777CrossRefGoogle Scholar
  116. 116.
    McCauley MJ, Rueter EM, Rouzina I, Maher III LJ, Williams MC (2012) Nucleic Acids Res 41:167PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Xiao B, Zhang H, Johnson RC, Marko JF (2011) Nucleic Acids Res 39:5568PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Zhang H, Marko JF (2010) Phys Rev E 82:051906CrossRefGoogle Scholar
  119. 119.
    Finzi L, Gelles J (1995) Science 267:378–380PubMedCrossRefGoogle Scholar
  120. 120.
    Splinter E, Heath H, Palstra RJ, Klous P, Grosveld F, Galiart N, de Laat W (2006) Genes Dev 20:2349–2354PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Marko JF, Siggia ED (1997) Mol Biol Cell 8:2217–2231PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Wood AJ, Severson AF, Meyer BJ (2010) Nature Rev Genet 11:391PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Strunnikov AV, Larionov VL, Koshland D (1993) J Cell Biol 123:1635PubMedCrossRefPubMedCentralGoogle Scholar
  124. 124.
    Hirano T, Mitchison T (1994) Cell 79:449PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Hirano T (2006) Nat Rev Mol Cell Biol 7:311PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Haering CH, Farcas A-M, Arumugam P, Metson J, Nasmyth K (2008) Nature 454:297PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Cuylen S, Metz J, Haering CH (2011) Nat Struct Mol Biol 18:894PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Murayama Y, Uhlmann F (2014) Nature 505:367PubMedCrossRefPubMedCentralGoogle Scholar
  129. 129.
    Kimura K, Hirano T (1997) Cell 90:625PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR (1999) Cell 98:239PubMedCrossRefPubMedCentralGoogle Scholar
  131. 131.
    Carter SD, Sjögren C (2012) Crit Rev Biochem Mol Biol 47:1PubMedCrossRefGoogle Scholar
  132. 132.
    Sun M, Nishino T, Marko JF (2013) Nucleic Acids Res 41:6149PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Strick T, Kawaguchi T, Hirano T (2004) Curr Biol 14:874PubMedCrossRefGoogle Scholar
  134. 134.
    Cui Y, Petrushenko ZM, Rybenkov VV (2008) Nat Struct Mol Biol 15:411PubMedCrossRefGoogle Scholar
  135. 135.
    Petrushenko ZM, Cui Y, She W, Rybenkov VV (2010) EMBO J 29:1126PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Sanborn AL, Rao SS, Huang SC, Durand NC, Huntley MH, Jewett AI, Bochkov ID, Chinnappan D, Cutkosky A, Li J, Geeting KP, Gnirke A, Meinikov A, McKenna D, Stamenova EK, Lander ES, Aiden EL (2015) Proc Natl Acad Sci USA 112:E6456-65PubMedCrossRefGoogle Scholar
  137. 137.
    Fudenberg G, Imakaev M, Goloborodko A, Abdennnur N, Mirny LA (2016) Cell Rep 15:2038–2049PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Hirano T (2005) Philos Trans R Soc Lond B 360:507CrossRefGoogle Scholar
  139. 139.
    Nasmyth K (2001) Annu Rev Genet 35:673–745PubMedCrossRefGoogle Scholar
  140. 140.
    Alipour E, Marko JF (2012) Nucleic Acids Res 40:11202PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, Aiden EL (2014) Cell 159:1665–1680PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Maeshima K, Eltsov M, Laemmli UK (2003) Chromosoma 114:365–375CrossRefGoogle Scholar
  143. 143.
    Goloborodko AA, Marko JF, Mirny LA (2016) Biophys J 110:2162–2168PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Goloborodko AA, Imakaev MV, Marko JF, Mirny L (2016) Elife 5:e14864PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Marko JF (2008) Chrom Res 16:469–497PubMedCrossRefGoogle Scholar
  146. 146.
    Marko JF (2012) The mitotic chromosome: structure and mechanics, ch. 18. In: Rippe K (ed.) Genome organization and function in the cell nucleus. Wiley-VCH, Weinheim, pp 449–486Google Scholar
  147. 147.
    X Wang, Brandao HB, Le TB, Laub MT, Rudner DZ (2017) Science 355:524–527PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Terakawa T, Bisht S, Eeftens JM, Dekker C, Haering CH, Greene EC (2017) Science 358:672–676PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Stephens AD, Banigan EJ, Adam SA, Goldman RD, Marko JF (2017) Mol Biol Cell 28:1984–1996PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Nathan D, Crothers DM (2002) J Mol Biol 316:7–17PubMedCrossRefGoogle Scholar
  151. 151.
    Pongor CI, Bianco P, Ferenczy G, Kellermayer R, Kellermayer M (2017) Biophys J 112:512–522PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Simon M, North JA, Shimko JC, Forties RA, Ferdinand MB, Manohar M, Zhang M, Fishel R, Ottesen JJ, Poirier MG (2011) Proc Natl Acad Sci USA 108:12711–12716PubMedCrossRefGoogle Scholar
  153. 153.
    Pommier Y, Leo E, Zhang H, Marchand C (2010) Chem Biol 17:421–433PubMedCrossRefGoogle Scholar
  154. 154.
    Fisher JB, McNulty M, Burke MJ, Crispino JD, Rao S (2017) Trends Cancer 3:282–293PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Spagnol ST, Armiger TJ, Dahl KN (2016) Cell Mol Bioeng 9:268–276PubMedPubMedCentralCrossRefGoogle Scholar
  156. 156.
    Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, Tewari M, Rehfeldt F, Speicher DW, Discher DE (2013) Science 341:1240104PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Davidson PM, Lammerding J (2014) Trends Cell Biol 24:247–256PubMedCrossRefGoogle Scholar
  158. 158.
    Stephens AD, Liu PZ, Banigan EJ, Almassalha LM, Backman V, Adam SA, Goldman RD, Marko JF (2017) Mol Biol Cell E17-06-0410Google Scholar
  159. 159.
    Hutchison CJ (2014) Adv Exp Med Biol 773:593–604PubMedCrossRefGoogle Scholar
  160. 160.
    Bennett RL, Licht JD (2018) Annu Rev Pharmicol Toxicol 58:187–207CrossRefGoogle Scholar
  161. 161.
    Banigan EJ, Stephens AD, Marko JF (2017) Biophys J 113:1654–1663PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Borsos M, Torres-Padilla ME (2016) Genes Dev 30:611–621PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Mulligan PJ, Koslover EF, Spakowitz AJ (2015) J Phys Cond Mat 27:064109CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Northwestern UniversityEvanstonUSA

Personalised recommendations